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Diversity and Ecology of Wild of Riparian Zone of Lake Kivu, Rwanda

By

Emmanuel MUNYANEZA

College of Sciences and Technology

School of Science

Master of Science in Biodiversity Conservation

and Natural Resources Management

2018

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Diversity and Ecology of Wild Mushrooms of Riparian Zone of Lake Kivu, Rwanda

Thesis submitted in partial fulfillment of the award of MSc degree in Biodiversity Conservation and Natural Resources Management

By

Emmanuel MUNYANEZA o Reg.N 215043178 In the College of Science and Technology

Supervisors: Prof. Elias BIZURU,University of Rwanda Dr. Jérôme DEGREEF, Fédération Wallonie-Bruxelles & Botanic Garden Meise (Belgium)

May 2018

DECLARATION

I declare that this thesis has been composed solely by myself and that it has not been submitted, in whole or in part, in any previous application for award of other degree. Except for quotations and summaries which have been acknowledged, the work presented is entirely my own.

Emmanuel MUNYANEZA

Reg.No 215043178

Signed

Date: 25/05/2018

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Certification

This is to certify that the Project Work entitled “Diversity and Ecology of Wild Mushrooms of Riparian Zone of Lake Kivu, Rwanda” is a record of the original bonafide work done by:

MUNYANEZA Emmanuel (REG.NO: 215043178)

in partial fulfilment of the requirement for the Degree of MASTER OF SCIENCE IN BIODIVERSITY CONSERVATION AND NATURAL RESOURCES MANAGEMENT in College of Science and Technology, University of Rwanda during the Academic Year 2017- 2018.

…………………….... ……………………...... Prof. Elias BIZURU Dr MUTANGANA Dieudonné Supervisor Head of Department of Biology

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ABSTRACT

Fungi are among the most diverse group of living organisms on earth, though inadequately studied worldwide and especially in Rwanda. The main objective of this study was to assess the diversity and describe the ecology of mushrooms species in Rwanda in order to develop a baseline that can help for further studies on fungi in the country.

The Macromycetes diversity and distribution of the riparian zone of Lake Kivu were studied by plot-based surveys at 3 study sites (Mariri, Mpangara and Nyakarwa) and simple random searches in the garden of the Museum of Environment, from September 2016 to June 2017. More than 64 mushroom species were recorded, collected, dried and their specimens are conserved in the Museum of Environment of Karongi, Rwanda. A total of 64 species were collected, belonging to 8 orders, 26 families and 40 genera. It was revealed that the riparian zone of Lake Kivu is dominated by , an order represented by 52 species, 81% of all species collected. The total order/family ratio of 0.31, family/ ratio of 0.65 and genus/species ratio of 0.63 is an indicator of high family and generic diversity in the collections. Families highly represented in collections with the most number of species are Agaricaceae with 18 species, Tricholomataceae with 10 species and Psathyrellaceae with 5 species. In this study, Termitomyces medius was collected and recorded for the first time in Rwanda. This study has provided 14 new records on the list of mushroom species in Rwanda. Moreover, the study has also provided other 43 potential new records which were identified to genus level. More number of mushrooms species was recorded in Nyakarwa Forest and Sorenson similarity matrix calculated showed dissimilarity richness and distribution of mushrooms species among 4 sites surveyed during this study. During the study period, the number of species present increased with rainfall. The most species were recorded and collected in December and decreased to 0 in the June dry season.

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KEY WORDS

Mushrooms, diversity, ecology, Lake Kivu, riparian zone.

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LIST OF SYMBOLS AND ACRONYMS

INMR: Institute of National Museums of Rwanda ITCZ: Intertropical Convergence Zone MINIRENA: Ministry of Natural Resources MINITERE: Ministère des Terres, de ’Environnement, des Forets, de l’eau et des Ressources Naturelles REMA: Rwanda Environment Management Authority USAID: United States Agency for International Development

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TABLE OF CONTENTS

Declaration...... i Certification…………………………………………………………………………………...ii Abstract ...... iii Key words………………………………………………………………………………...…. iv List of symbols and acronyms ………………………………………………………………..v List of tables ...... vii List of figures ...... viii 1. Introduction ...... 1 2. Materials and Methods………….. ……...... 4 2.1. Description of study sites...... 4 2.2. Data collection and analysis...... 6 3. Results ...... 8 3.1. Species richness within Macrofungi...... 8 3.2. Species distribution and ecology………………………...... 10 3.3. Potential use of recorded mushrooms species…………………………………………...13 4. Discussion ...... 14 5. Conclusion and recommendations ...... 18 Acknowledgement………………………………………………………………………… .19 Bibliography ...... 20 Appendices...... 24

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LIST OF TABLES

Table 1. Scales used in rating mushrooms species frequency…………..…………………7

Table 2. Total number of families, genera, species and percentage of species collected in this study………………………………………………………………….…. 9 Table 3. Sorenson’s similarity matrices for species distribution in study sites………….…11

Table 4. List of species with their potential uses……………………………………….…..13

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LIST OF FIGURES

Figure 1. Orders and ampleness of mushrooms families in riparian zone of Lake Kivu…….8 Figure 2. Richness of species, genera, families and orders in study sites ……………..… 10 Figure 3: Frequency distribution of species in study sites ……………..…………………. 10 Figure 4. Frequency distribution of mushrooms species in whole study region ……… 11

Figure 5. Monthly recorded species numbers in different study sites ………...……………12

Figure 6. Distribution of mushroom species in different habitat typ ……………………….12

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1. Introduction

The biological diversity of Rwanda is well conserved and protected within protected ecosystems (REMA, 2014b; USAID, 2014) while no or less consideration is given to non- protected ecosystems. However, as it was mentioned by some authors, conserving the national or regional biodiversity only in protected areas and National Parks, is a strategy unlikely to succeed, because they don’t cover all proportional type of habitat of national or regional biodiversity ( Hayes & Ostrom 2005;Cai et al. 2009; Cox & Underwood 2011).

Various scientific and government reports on national biodiversity have revealed that Rwanda hosts natural ecosystems with large biological diversity ( Stuart et al. 1990; Plumptre et al. 2003; MINIRENA 2011; REMA 2014b). The diversity of natural ecosystems found in Rwanda include Afromontane forests, savannas, gallery forests, riparian zones, wetlands and lakes (REMA, 2010, 2014b). As it has been reported in the Fifth National Report to the Convention of Biological Diversity (REMA, 2014b) the status and trend of biological diversity in Rwanda vary from one ecosystem to another and the human-induced landscape changes are pressing more on non-protected areas than on National Park and other protected areas. However, some research done in various remnant natural ecosystems in Rwanda have already revealed that some interesting and rare species are persisting in small remnant natural habitats separated by intensive agricultural and urban areas (Kanyamibwa 1997; Nsabagasani et al. 2008; Bizuru et al. 2011; Fischer 2011; REMA 2014a). During the biodiversity survey done in Lake Kivu islands (REMA, 2014a), it was revealed also that this area constitutes a refugia area of damaged zones of the main land and are home to different plants and animals species which some of them having a particular status of being endemic or endangered, like Atilax palutinosus and water bird species. Although the survey did not consider riparian zone of Lake Kivu, the vegetation structure and vegetation composition of Lake Kivu islands and riparian zones are very similar and they could have similar biological diversity. The riparian zone should have another ecological advantage as it is connected to adjacent upland and plays the role of corridor and refuge for all surrounding biodiversity (Goforth et al., 2002).

Like many other research and biodiversity surveys done in Rwanda, in the survey done by REMA (REMA, 2011, 2014a) mushroom species were ignored and not considered among biodiversity living organisms to be surveyed. According to Egbe Enow et al. (2013), mushrooms are not taken into consideration in many research works due to their largely

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hidden nature and frequently sporadic and short-lived sporocarps. Despite this kind of ignorance by research, mushrooms constitute a significant part of terrestrial ecosystems, forming a large share of the world biodiversity richness and are key-players in ecosystem processes ( Molina 1994; Halme 2012). In general, Fungi is one of largest group of organisms on the Earth with an estimated number of 1.5 million species (Hawksworth, 2001; Osemwegie, Okhuoya and Dania Akande, 2014) and it occupies the second place after insect with about 8 million of species (Hawksworth, 2002). It is also estimated that only about 8- 10% of the 1.5 million species have been described and most of them, are in temperate regions; the tropical region which is undoubtedly hosting the highest fungi diversity has been inadequately sampled and scarcely documented (Hawksworth 2001; 2002). Moreover, mushrooms are also currently highly threatened by habitat loss, pollution, over-exploitation and climate change ( Osarenkhoe et al. 2014; Degreef et al. 2016).

Although the taxonomic knowledge of fungi is very incomplete and their ecology has not yet been studied, some preliminary observations on the taxonomic diversity and ecology have shown that the African tropical region should be a hotspot of endemic species (Verbeken and Buyck, 2002). Central and East African regions, which are known to be a hotspot of biological diversity, host a big number of mushrooms species (Buyck, 1994; Chelela, Chacha and Matemu, 2015; Degreef et al., 2016). Despite that mycological richness of Africa, till now only one research study has been done on diversity and ecology of mushrooms in Rwanda (Degreef et al. 2016). This study only focused on edible species and was restricted to montane forest ecosystems. However, as it has been found in previous research works that the distribution of many African fungi are linked to the contrast between open woodlands and dense forests (Buyck 1994; Verbeken & Buyck 2002; Djelloul & Samraoui 2011). Based on habitat structure of riparian zone of Kivu Lake, riparian forest of evergreen forest densely populated by native tree species, woodland and herbaceous layer of grass savannah; those different vegetation types should host different mushroom species associated with different habitat structure and linked to ecological requirement of each species.

Riparian zones and islands of Kivu Lake, are ones of remnant natural habitats which are not yet included in biodiversity conservation policy in Rwanda while its species richness is high and specific (REMA, 2011, 2014a). High biodiversity of riparian zones is due to the fact that they encompass sharp environmental gradients and diverse ecological processes (Goforth et al. 2002; Olson et al. 2007; Henson et al. 2010). Therefore, riparian zones and islands should be potential habitats for sustaining a significant portion of national biodiversity in Rwanda

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based on consideration of Gregory et al. (1991) underlining that riparian zones act as biodiversity refugia while the disturbance and fragmentation of adjacent upland are intensified.

Despite high biological richness of the country, all research works have focused only on plants and animals. Fungi have always been forgotten or ignored and are not included in any scientific report on biological diversity of Rwanda or of Albertine Rift Region. Existing information on fungal diversity and composition in the country is very poor. Thus, it is highly imperative to assess fungal diversity and species composition of different habitats and ecosystems. Therefore, this study was designed with the aim of addressing general lack of information pertaining to mushroom diversity with a view to attract attention of policy makers to integrate riparian zones and mushroom species in biodiversity conservation strategies and to increase the knowledge of edible and medicinal mushroom resources of the country.

The general objective of this study is to assess mushroom species found in the riparian zones of Lake Kivu and to identify ecological factors that influence mushroom distribution in different habitat types within this zone. The specific objectives of this study are (1) to contribute to the inventory of mushrooms species of Rwanda; (2) to identify ecological factors related to mushroom species distribution in study sites; (3) to collect and preserve mushrooms specimens from the study area and finally (4) to compile data on traditional uses in the region (neighbouring countries) of mushrooms species identified.

To achieve the mentioned objectives, the following research questions were formulated: What are mushroom species that are correlated with different habitat types and the ecological condition of the riparian zone of Kivu Lake? Is there any similarity of species distribution across different habitat types? What are the potential uses of mushroom species occurring in this region? The central hypothesis of the study was that the riparian zone of Lake Kivu hosts specific mushroom species. We expected that the mushrooms species found in this region have multiple uses that we have to document, popularize and include in potential ecosystem services of this zone.

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2. Materials and Methods

2.1. Description of study sites

The riparian zone of Lake Kivu constitute one of natural habitats of the Albertine Rift region, in western province of Rwanda and this region is an area of high endemism and threatened species (Plumptre et al., 2003). Lake Kivu is located at the topographic high point of the western branch of the African Great Rift Valley, at 1463 m above mean sea level (Wood, 2014). The riparian zones and surrounding areas of Lake Kivu, like all other ecological zones of the country, benefit from a continental tropical humid climate with alternating dry and rain seasons. This alternation is due to a bimodal rainfall pattern that Rwanda experience, driven by the progression of the Inter-Tropical Convergence Zone (ITCZ) (McSweeney, 2011). Therefore, Rwanda is characterized by 4 seasons: short dry season in January to February, long rains season occurring over March- May, long dry season from June to August and short rains season in October to December (McSweeney, 2011). Riparian zones of Kivu Lake, where the study sites are located, receive annual rainfall from 1100-1200 mm with mean annual temperature ranging between 18 and 20oC (MINITERE, 2007). The study sites included, the garden of Museum of Environment in Karongi, Mariri Peninsulas, Mpangara Island and the Nyakarwa Forest. Mpangara Island and Mariri Peninsula were chosen for their topography which facilitates accessibility for most vegetation types. Since 2015 the two sites are managed as protected forests (Official Gazette n0 27 of 06/07/2015 on Ministerial Order No 006/Minirena/2015 of 18/06/2015 determining the management of protected state forests not governed by special laws). The status of protected forest is a good factor for research site allowing continuous research activities. Nyakarwa Forest was chosen due to its vegetation structure which is special and unique on the mainland adjacent to Lake Kivu riparian zone with a mixture of local and exotic tree species, large amounts of litter, and biodegradable organic matter.

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Photo a: Nyakarwa Forest Photo b: Mariri Woodland

Photo c. Mpangara Island

Mpangara Island is an island of 2.57 ha, located in Karongi District. The vegetation type of this island is composed of riparian woodland layer of indigenous plant species (Ficus ingens, Rhus natalensis, Carissa edulis, Carissa spinarum) and some exotic plant species (Eucalyptus ssp. and Grevillea robusta). The island also has a shrub layer dominated by Lantana camara, an exotic plant species, some local species including Lantana trifolia, Rhus natalensis, and savannah grassland.

Mariri Peninsula is located in Bwishyura Sector, Karongi District. It is a peninsula of 3.12 ha characterized by a woodland layer on the shores of Lake Kivu and woodland savannah and grassland layer upward. The riparian woodland is dominated by indigenous plant species including Ficus ingens, Acacia hockii, Phoenix reclinata and Euphorbia candelabrum. Lantana camara tend also to invade this natural habitat.

Nyakarwa Forest is about 4 ha and is known as “Agashyamba ka Nyakarwa” by local residents which means forest located on island. The vegetation of that forest is dominated by many indigenous plant species (Euphorbia candelabrum, Harungana madagascariensis, Dodonea viscosa, Phoenix reclinata, Ochna holstii etc) with a canopy of exotic species (Casuarina equisetifolia, Eucalyptus ssp. and Jacaranda mimosifolia). The forest also shelters important indigenous herbaceous and bryophytes species.

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The garden of the Museum of Environment is located in Karongi District at the shores of Lake Kivu. This garden is covering an area of about 0,5 ha and the whole area is almost covered by Paspalum notatum. In the Paspalum's gazon some exotic and local ornamental trees, shrubs and herbs are planted to embellishing the garden.

2.2. Data collection and analysis

A reconnaissance survey was conducted during April-May 2016 to get an insight of the vegetation pattern and topography in order to locate sampling plots. A total of 18 plots (10m x10m), six from each site (Mariri, Mpangara and Nyakarwa), were established and sampled. Because the museum garden is small and very easy to survey all its corners, fruiting bodies were collected randomly all over in the garden during study period. Plots were established randomly in each vegetation structure according to the accessibility of site. This is the best method recommended in the areas with stratified vegetation structure and allows the collection of data on diversity and comparison of abundance and diversity between habitat structures ( Kenkel et al. 1989; Hill et al. 2005; Moore et al. 2011).

All mushroom species found in plots and garden were recorded, photographed and collected. All ecological data of each species found were also recorded. Ecological data includes habitat, substrates (i.e. dead wood, standing trees, termite mount, soil and litter). The plots were surveyed using presence-absence for fruit bodies of mushroom in systematic placement for the coverage of plots as it is recommended by Lodge et al. (2004); Hill et al.( 2005) and Halme (2012) , twice a month from September 2016 to June 2017. Fruit bodies were collected, and each specimen was described when fresh (size, shape, colour, hymenium or details of the spore bearing surface) and all specimens were separated into species and/or genus by identifying their characters according to the keys and reference guides (Buyck 1994; Eyi Ndong et al. 2011; De Kesel et al. 2017; Degreef and De Kesel, 2017) . Specimens collected were dried and preserved using standard methods (Eyi Ndong et al. 2011) and constitute the basic data of museum herbarium and the duplicates will be sent to the Herbarium of Botanic Garden Meise in Belgium.

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The frequency of species, represented by the number of plots in which a species was recorded was computed for each site. Species similarity between sites was determined using the Sorenson’s coefficients and Chao 2 estimator was used for estimating omitted species (Hill et al., 2005; Marcon, 2006). The relative dominance and relative density was calculated by the following formula(Cottam & Curtis 1956).

Relative frequency = Number of plots containing species x in Site n x 100 Total number of plots in site n

Relative density = Number of species of family x in site n x 100 Number of species of all families in Site n

The following frequency classes were used to designate the frequency status of each species in different study sites and in the whole region covered by this study. The species frequency indicates the number (%) of plots in which the species has been recorded

Table 1. Scales used in rating mushrooms species frequency

Scale Rating Description

1 Rare Species with relative frequency < 20%

2 Occasional Species with relative frequency between 21% and 49 %

3 Frequent Species with relative frequency between 50% and 74%

4 Abundant Species with relative frequency > 75%

Ethnomycological data had been gathered through survey and literature review. The information on edibility of some recorded species is mostly obtained from the population surrounding the study areas including people that we met in bushes and forest collecting firewood and a group of population that have been expropriated from some Kivu islands. The uses of different species in other communities and countries have been gathered from available literature.

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3. Results

3.1. Species richness within Macrofungi

The riparian zones of Kivu Lake are dominated by Agaricales, an order represented by 52 species among 64 species which means 81% of all species collected. Agaricales are followed by with 4 species (6%), Geastrales and Polyporales with 2 species for each (3%) while other orders are represented by one species.

A total of 64 species collected from all four study sites, Mariri, Mpangara, Nyakarwa and INMR garden belong to 8 orders, 26 families and 40 genera. The total order/family ratio of 0.31, family/genus ratio of 0.65 and genus/species ratio of 0.63 indicates the total high family and generic diversity in the collections. The families highly represented in collections with the most number of species are Agaricaceae with 18 species, Tricholomataceae with 10 species, Psathyrellaceae with 5 species and Strophariaceae with 4 species. Those 4 families account for more than 50% of collected species whereas Lyophyllaceae is represented by 3 species, Boletinellaceae, Geastraceae and Marasmiaceae are each represented by 2 species. Other 18 families are each represented by only one species. Table 2, shows the total number of families, genera, species and relative density of species collected in this study. The full list of species collected and identified in this study is presented in Appendix 1 while appendix 4 shows their photos. Appendix 3 shows the provisional list of mushrooms species recorded in Rwanda.

Figure. 1. Orders and ampleness of mushrooms families in riparian zones of Lake Kivu.

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Table 2. Total number of families, genera, species and relative density of species collected in this study.

No. Family name Number Number Relative of Genera of Species density % 1 Agaricaceae 7 18 28.13 2 Amanitaceae 1 1 1.56 3 Bolbitiaceae 1 1 1.56 4 Boletinellaceae 2 2 3.13 5 Cantharellaceae 1 1 1.56 6 Entolomataceae 1 1 1.56 7 Ganodermataceae 1 1 1.56 8 Geastraceae 2 2 3.13 9 Gomphaceae 1 1 1.56 10 Hygrophoraceae 1 1 1.56 11 Hygrophoropsidaceae 1 1 1.56 12 Inocybaceae 1 1 1.56 13 Lyophyllaceae 1 3 4.69 14 Marasmiaceae 1 2 3.13 15 Mycenaceae 1 1 1.56 16 Nidulariaceae 1 1 1.56 17 Pleurotaceae 1 1 1.56 18 Pluteaceae 1 1 1.56 19 Polyporaceae 1 1 1.56 20 Psathyrellaceae 2 5 7.81 21 Repetobasidiaceae 1 1 1.56 22 Russulaceae 1 1 1.56 23 Schizophyllaceae 1 1 1.56 24 1 1 1.56 25 Strophariaceae 2 4 6.25 26 Tricholomataceae 5 10 15.63

Among all mushroom species recorded and collected during this study in riparian zones of Lake Kivu, a high number of species was recorded from Nyakarwa Forest with 40 species (16 families and 6 orders). (Figure 2).

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Figure 2. Richness of species, genera, families and orders in study sites

3.2. Species distribution and ecology

The frequency of occurrence of species recorded during this study in each study site is presented in Figure 3 and Figure 4 show the overall frequency of occurrence of species if we consider the whole region covered by our study which means all sites together including museum garden.

Figure 3. Frequency distribution of species in study sites

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Figure 4. Frequency distribution of mushrooms species in whole study region

The similarity of species distribution in study sites was calculated using Sorenson’s similarity matrices and the results are shown in the Table 3.

Table 3. Sorenson’s similarity matrices for species distribution in study sites

Nyakarwa Mariri Mpangara INMR Garden

Nyakarwa 1 Mariri 0.39 1 Mpangara 0.36 0.11 1 INMR Garden 0.36 0.24 0.16 1

The number of species recorded during study period varied according to rainfall received in the region. The number of species seems clearly correlated with the rainy season. The most species were recorded and collected in December and decreased to 0 in dry season from June (Figure 5).

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Figure 5. Monthly recorded species numbers in different study sites

Vegetation structure play a big role on mushroom distribution, most species have been recorded and collected in forest, followed by woodland, garden and grassland (Figure 6).

Figure 6. Distribution of mushroom species in different habitat types.

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3.3. Potential use of recorded mushrooms species

Information from field survey on uses of wild mushrooms in Karongi region has revealed that only 3 species of mushrooms are known and used as edible mushrooms. These species belong to Termitomyces genera and are Termitomyces medius, Termitomyces microcarpus, and Termitomyces robustus. All others species are considered as toxic and poisonous. However, among species recorded in study area about 14 species are known to be edible in other countries and 3 species are used in traditional medicine (Table 4).

Table 4: List of species with their potential uses

Species Uses Country References Agaricus crocopeplus Edible Tanzania Tibuhwa, 2012

Collybia piperata Edible D R Congo Eyi Ndong et al. 2011 Cotylidia aurantiaca Edible Burundi,D R Congo , Degreef et al. 1997; Degreef Rwanda et al. 2016 Gymnopilus zenkeri Edible Cameroun, Gabon, Eyi Ndong et al. 2011 Malawi, Ouganda Lentinus Edible R of Centrafrique, D R Eyi Ndong et al. 2011 brunneofloccosus Congo, Gabon, Ghana Macrolepiota africana Edible Cameroun, R of Degreef et al. 1997; Degreef Centrafrique, D R et al. 2016; Eyi Ndong et al. Congo, Gabon, Kenya, 2011 Rwanda Macrolepiota procera Edible Gabon, D R Congo, Degreef et al. 1997; Eyi Nigeria, Tanzanie Ndong et al. 2011; Hussein et al. 2015; Okoro & Achuba 2012 Medicine Tanzania Hussein et al. 2015; Tibuhwa (Wound, 2012 Antimicrobial) Marasmius arborescens Edible Angola, Burundi, D R Degreef et al. 2016; Eyi Congo, Rwanda Ndong et al. 2011 Schizophyllum commune Edible Gabon, D R Congo, Degreef et al. 1997; Eyi Nigeria, Tanzania, Ndong et al. 2011; Eyi Ndong et al. 2014 Medicine Nigeria Oyetayo 2011 (Diabete) Suillus granulatus Edible Rwanda Degreef et al. 2016 Termitomyces medius Edible Rwanda Present study

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Species Uses Country References

Termitomyces Edible Burundi, Gabon, D R Buyck 1994; Chelela et al. microcarpus Congo, Cameroun, 2015; Degreef et al. 1997; Uganda, Tanzania, Degreef et al. 2016; Opige, Rwanda M., Kateyo, E., Kabasa, J. D., Olila 2006 Medicine Nigeria, Tanzania Oyetayo 2011 (Gonorrhea) Medicine Tanzania Tibuhwa 2012 (Lactogen) Termitomyces robustus Edible Burundi, Nigeria, DR Buyck 1994; Eyi Ndong et al. Congo, Cameroun, 2014; Eyi Ndong et al. 2011; Uganda, Gabon, Degreef et al. 2016 Rwanda Volvariella volvacea Edible Gabon, Nigeria Eyi Ndong et al. 2011; Eyi Ndong et al. 2014; Okoro & Achuba 2012 Medicine Nigeria (Antibiotic) Oyetayo 2011

4. Discussion

The results of this study are the first for such systematic survey and inventory of wild macromycetes diversity in Rwanda. Among study sites surveyed, significant high number of species was collected in Nyakarwa Forest during the study period, where 40 species belonging to 18 genera in 16 families were recorded. Nyakarwa forest is followed by Mariri in species richness with 26 species belonging to 18 genera and 16 families (Figure.3).

The high level of Nyakarwa fungal diversity may be attributed to a closed canopy of its vegetation and biodegrading ability of many recalcitrant substrates found in that forest. This result is in agreement with Verbeken & Buyck (2002), Gómez-Hernández & Williams-Linera (2011), and Sandhya et al. (2017) ,that have highlighted the correlation of these ecological features with mushrooms abundance in their study sites. The biggest number of mushroom species of Mariri was also recorded in riparian woodland and was collected on organic materials, decomposing plant litter and decaying shrubs. Only 7 species were collected in the grassland habitat, Cotylidia aurantiaca, Gymnopilus zenkeri, Parasola plicatilis,

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sudanicus, Pholiota sp., Schizophyllum commune and Suillus granulatus. The lowest species richness of Mpangara Island could be due to its location of being isolated from mainland.

The high frequency of Agaricaceae family in study sites is attributed to adaptability of the species of this family in tropical areas and this is in agreement with the results obtained from other studies in tropical areas (Kebede, 2017; Megersa et al., 2017; Sandhya, Surendra and Kumar, 2017). The dominance of species of this family is due to their efficient dispersal mechanisms and adaptation to ecological conditions (Hawksworth, 2001; Kebede, 2017). Tibuhwa (2012) underlined that species of Agaricaceae were also the most common species and were used by communities around Ngorongoro and Serengeti National Park in Tanzania. Apart the explanation given by these authors mentioned above, there is no other convincing reason to explain the high abundance of Agaricaceae family in this region in comparison to other fungi families. As they are well distributed in all habitat types it is an indicator that it must be a special link between ecological requirements of species members of this family and ecological features of this region. Therefore, a further study is needed to evaluate the correlation of the presence of Agaricaceae in this region and its ecological features.

The distribution of mushroom species in four study sites ( Museum garden, Mariri, Mpangara and Nyakarwa) are relatively less similar, Sorenson’s similarity index ≤ 0,39. The mushroom species collected in Nyakarwa Forest are distributed in other three study sites with Sorenson’s similarity index of 0,36 and 0,39. The similarity of Nyakarwa and other sites should be attributed to the fact that this site represent all ecological features of Kivu riparian zone and most species distributed in different sites of this zone are present in Nyakarwa Forest. The sites which are very dissimilar are Mpangara and Mariri, with a similarity index of 0,11 (Table 3).

The difference in species richness between Mpangara Island and the Mariri Peninsula is somewhat surprising because the structure of the natural vegetation of these two habitats is very similar. The dissimilarity in species richness may be caused by their location: the isolation from mainland of Mpangara as it is an island while Mariri is a peninsula. This assumption is supported by previous results showing the effect of isolation on the distribution and abundance of species. Peay et al. (2007), Henson et al. (2010) and Jones et al. (2016) have highlighted that isolation decreases species richness by reducing the number of potential colonists dispersing into an area and as consequence many islands lack species common on

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the mainland while they can support other species in great abundance, or harbour species largely restricted to islands given their land area.

During the study period, the frequency occurrence of species in each habitat was found to be different. In all study sites, occasional species made most of the collection and the distribution of dominant species were very low (Figure 4 and Figure 5). The fact that most species recorded are ranged from rare and occasional species indicates that species distribution varies with vegetation structure. More species were collected in plots located in forest (Figure 8). On the other hand, the methodology used, surveying twice a month, may lead to the missing of some records as the fructification of most mushroom species occur at different times, although the value of the Chao2 estimator calculated (64 + 3.6) was moderate.

Most of the species were recorded in forest habitat, followed by woodland, garden and finally grassland. Most species recorded are saprotrophic and were recorded in plots with dead organic materials, decomposing plant litter and decaying wood.

Due to ephemeral fruiting bodies that can be observed only for few days, phenological data is difficult and time consuming to obtain results with high exactitude level. However, in this study, a large number of records were correlated with precipitation. The most species were recorded and collected in November and December in the first rainy season (Agricultural season A) and in April and May in the second rainy season (Agricultural season B) (Figure 6 and Figure7). Comparing two rainy seasons, most mushroom collections were observed in November-December than in March-May. This difference can be due to many factors including phenological period of species occurring in this region and variation of rainfall received in each season. A further study extending over long study period and taking into account the rainfall variation may provide more information about fruiting period of each species and assess whether there is any correlation between species abundance and seasons.

Among 64 species recorded in this study, only 3 species of Termitomyces have been reported to be edible by local community. Those species are Termitomyces medius, Termitomyces microcarpus and Termitomyces robustus. The population of Karongi don't consider mushrooms as a principal source of food; they use them occasionally if they found them in their field. However, among species collected, there are about 14 species known to be edible in other countries including neighbouring countries, Burundi, Tanzania, Uganda and Democratic Republic of Congo (Table 4). To differentiate edible mushrooms to non-edibles

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ones, the local population use a common name of " Ibihegehege" for non-edible mushroom while each edible species has a specific vernacular name. Indenganzira is the vernacular name of Termitomyces medius, Imegeri is the vernacular name of Termotomyces microcarpus and Igihumyo or Icyobo are the vernaculars names of Termitomyces robustus. Termitomyces medius was collected once in November and has been recorded and reported by an ethno mycological study for the first time as edible mushroom in Rwanda during this study.

As saprophytic mushrooms are found growing on rotten logs of woody tree trunks, decaying or dead organic matter, and dump soil rich in organic substances, some wild species are subject of research work for growing them on artificial medium. Among saprophytic edible species, Volvariella volvacea and other two species belonging to Coprinus and Pleurotus genera ( Coprinus cinereus, Pleurotus flabellatus) have been grown on agricultural and agro- industrial residues as substrate by different scientists and the results were interesting (Apetorgbor et al. 2005; Mshandete & Cuff, 2008) . Therefore, some species recorded in this zone including Volvariella volvacea, Coprinus sp. and Pleurotus sp. can also be subject of research work focusing to grow them on artificial medium in order to improve their production and generating a great socio-economic impact in human welfare on local level.

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5. Conclusion and recommendations

The present study is an attempt to provide a preliminary picture of mushroom diversity in Rwanda, especially of riparian zones of Kivu Lake, and occurring in diverse natural habitat including woodland, grassland savannah and riparian forest. The list of mushrooms species collected and recorded in this study provides a baseline of information for further assessment on macrofungal diversity of the country. On the list of 37 species recorded by Degreef et al. (2016) in Rwanda, this study has provided additional records, 14 records identified to species level and 43 potential records identified to genus level (worth identification to species level) (Appendix 3). Record of the rare Termitomyces medius only known from Zambia and DR Congo is also an additional record among edible mushroom of Rwanda reported by an ethnomycological study.

The distribution of species in study sites surveyed, has led to think about several viewpoints to consider as main causes of unequal distribution and dissimilarity in species richness between sites. The diversity of habitat structure is believed to have the strongest impact on mushrooms species richness and distribution in surveyed sites. The habitat structure influences the quality of substratum then the mushroom diversity according to species ecology.

Though the full spectrum of mushroom diversity of the country is still far from being described and documented, these results on mushrooms occurrence in riparian zone of Lake Kivu, provide opportunities to forward conservation plan involving mushrooms as other living organisms that need a special consideration in biodiversity conservation program. Thus, it is highly recommended for further insight into mushrooms species composition and distribution in different ecological zones and habitat types of Rwanda with more in-depth studies namely on ecological aspects (host-plants for ectomycorrhizal species, substrate for saprotrophic species and soil type as an ecological correlate for species presence). The assessment survey should be combined with ethnomycological studies to highlight species with special cultural and economic values for community. The survey and research should also focus on species with potential ability to be grown on an artificial medium. As mushrooms cultivation does not require big space and good soil, cultivation of local species should generate income for many smallholder farmers in Rwanda and improve food security and quality in the country.

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Acknowledgment

This study was made successful by the generous support of many individuals. First of all, I am heartily thankful to my supervisors, Prof. Elias Bizuru (University of Rwanda) and Dr. Jérôme Degreef (Fédération Wallonie-Bruxelles & Botanic Garden Meise, Belgium), whose encouragement, guidance and support from the initial to the final level enabled me to develop an understanding of the subject. My sincere appreciation is extended to Prof. Donat Nsabimana, Prof. Beth Kaplin, Dr. Callixte Gatali and all lecturers involved in the Program of Biodiversity and Natural Resources Management for their contribution to this work. I acknowledge the support and assistance of authorities and staff of the Institute of National Museums of Rwanda, my classmates and field assistant during this study. Lastly, I offer my regards and blessings to my family and to all of those who supported me in any respect for the completion of this thesis.

Emmanuel MUNYANEZA

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Bibliography

Apetorgbor, M. M., Apetorgbor, A. K. and Nutakor, E. (2005) ‘Utilization and cultivation of edible mushrooms for rural livelihood in Southern Ghana’, 17th Commonwealth Forestry Conference, pp. 1–22.

Bizuru, E. et al. (2011) Inventory and mapping of threatened remnant terrestrial ecosystems outside protected areas through Rwanda. REMA. Kigali, Rwanda.

Buyck, B. (1994) Ubwoba: Les champignons comestibles de l’Ouest du Burundi. Bruxelles: AGCD.

Cai, M., Pettenella, D. and Padova, U. (2009) ‘Protection outside protected areas : How are farming systems influencing biodiversity conservation in Natura 2000 areas ?’, pp. 1–12.

Chelela, B. L., Chacha, M. and Matemu, A. (2015) ‘Wild Mushrooms from Tanzania : Characterization and their Importance to the Rural Communities’, Current Research in Environmental & Applied Mycology, 5(4), pp. 307–321. doi: 10.5943/cream/5/4/2.

Cottam, G. and Curtis, J. T. (1956) ‘The Use of Distance Measures in Phytosociological Sampling’, Ecology, 37(3), pp. 451–460. doi: 10.2307/1930167.

Cox, R. L. and Underwood, E. C. (2011) ‘The importance of conserving biodiversity outside of protected areas in mediterranean ecosystems’, PLoS ONE, 6(1). doi: 10.1371/journal.pone.0014508.

Degreef, J. et al. (1997) ‘Edible mushrooms of the Zambezian woodland area: A nutritional and ecological approach’, Biotechnol, Agron. Soc. Environ., 1(3), pp. 221–231.

Degreef, J. et al. (2016) ‘Wild edible mushrooms , a valuable resource for food security and rural development in Burundi and Rwanda’, Biotechnol, Agron. Soc. Environ., 20(4).

Degreef, J. and De Kesel, A. (2017) 'The Edible Fungi of Tropical Africa annotated database. Available at: www.EFTA-online.org (Accessed: 1 December 2017).

Djelloul, R. and Samraoui, B. (2011) ‘Distribution and ecology of the superior mushrooms of the Aulnaie of Ain Khiar ( El Kala National Park , Northeastern Algeria )’, African Journal of Environmental Science and Technology Vol., 5(6), pp. 448–456. doi: 10.5897/AJEST10.242.

Egbe Enow, A. et al. (2013) ‘Diversity and distribution of macrofungi ( mushrooms ) in the Mount Cameroon Region’, Journal of Ecology and the Natural Environment, 5(10), pp. 318– 334. doi: 10.5897/JENE2013.0379.

Eyi Ndong, H. et al. (2014) ‘Variation of the Consumption of Mushrooms by Pygmies and Bantus in the North of Gabon’, Advances in Microbiology, 4(December), pp. 1212–1221.

Eyi Ndong, H., Degreef, J. and De Kesel, A. (2011) ‘Champignons comestibles des forêts denses d ’ Afrique centrale Taxonomie et identifi cation’, Abc Taxa, 10, p. 254.

Fischer, E. (2011) Biodiversity Inventory for Key Wetlands in Rwanda Final Report. Kigali, Rwanda.

20

Goforth, R. R. et al. (2002) Biodiversity analysis of selected riparian ecosystems within a fragmented landscape. Michigan State University.

Gómez-Hernández, M. and Williams-Linera, G. (2011) ‘Diversity of macromycetes determined by tree species, vegetation structure, and microenvironment in tropical cloud forests in Veracruz, Mexico’, Botany, 89(3), pp. 203–216. doi: 10.1139/B11-007.

Gregory, S. V. et al. (1991) ‘An Ecosystem Perspective of Riparian Zones’, BioScience, 41(8), pp. 540–551. doi: 10.2307/1311607.

Halme, P. (2012) ‘Monitoring fungal biodiversity- towards an integrated approach’, Elsevier, pp. 1–9. doi: 10.1016/j.funeco.2012.05.005.

Hawksworth, D. L. (2001) ‘The magnitude of fungal diversity: the 1.5 million species estimate revisited’, Mycological Research, 105(12), pp. 1422–1432. doi: 10.1017/S0953756201004725.

Hawksworth, D. L. (2002) ‘Why Study Tropical Fungi ?’, Tropical Mycology, 2, pp. 1–11.

Hayes, T. and Ostrom, E. (2005) ‘Conserving the world’s forests: are protected areas the only way’, Indiana Law Review, 38(3), pp. 595–617. doi: 10.1525/sp.2007.54.1.23.

Henson, L. B. et al. (2010) Islands of Life : A biodiversity and Conservation Atlas of Great Lakes Islands, Nature of Conservation of Canada. Ontarion: Naturre Conservation of Canada.

Hill, D. et al. (2005) Handbook of Biodiversity Methods: Survey, Evaluation and Monitoring, Cambridge. Cambridge University Press. doi: 10.1017/CBO9780511542084.

Hussein, J. M. et al. (2015) ‘Antioxidant properties of seven wild edible mushrooms from Tanzania’, African Journal of Food Science, 9(9), pp. 471–479. doi: 10.5897/AJFS2015.1328.

Jones, I. L. et al. (2016) ‘Extinction debt on reservoir land-bridge islands’, Biological Conservation. Elsevier Ltd, 199, pp. 75–83. doi: 10.1016/j.biocon.2016.04.036.

Kanyamibwa, S. (1997) ‘Important Bird Areas in Africa and associated islands-Rwanda’, Important Bird Areas in Africa and associated islands, pp. 703–710. doi: 10.1016/S0006- 3495(64)86921-6.

Kebede, R. S. (2017) Morphological and Molecular Characterization , Diversity and Ethnomycological Studies on Wild Mushrooms of Central and Northwest Ethiopia. Addis Ababa University.

Kenkel, N. C. et al. (1989) ‘On sampling procedures in population and community ecology’, Vegetatio, 83(1–2), pp. 195–207. doi: 10.1007/BF00031692.

De Kesel, A., Kasongo, B. and Degreef, J. (2017) Champignons comestibles du Haut- Katanga ( R . D . Congo ).

Lodge, D. J. et al. (2004) ‘Collecting and Describing Macrofungi’, Biodiversity of Fungi: Inventory and Monotoring Methods, pp. 128–158.

21

Marcon, E. (2006) Mesures de la biodiversité, UMR. Available at: http://www.ecofog.gf/Docs/PFDA/MesuresBiodiv%0Aersite.pdf.

McSweeney, R. (2011) Rwanda s Climate : Observations and Projections. Oxford, United Kingdom.

Megersa, S. et al. (2017) ‘Macrofungi species richness and diversity in Dagaga and Gambo plantation and natural forests of Arsi Forest Enterprise, Oromia, Ethiopia’, Imperial Journal of Interdisciplinary research, 3(1), pp. 1681–1686.

MINIRENA (2011) Rwanda Biodiversity Policy, Republic of Rwanda. Kigali, Rwanda.

MINITERE (2007) Profil environnemental du District de Karongi. Kigali, Rwanda.

Molina, R. (1994) ‘The role of mycorrhizal symbioses in the health of giant redwoods and other forest ecosystems’, USDA Forest Service General Technical Report, PSW-151, pp. 78– 81.

Moore, D., Robson, G. D. and Trinci, A. P. J. (2011) ‘21st Century Guidebook to Fungi OUTLINE’, Outline Classification of Fungi, pp. 1–21. doi: 10.1017/CBO9780511977022.

Mshandete, A. and Cuff, J. (2008) ‘Cultivation of three types of indigenous wild edible mushrooms: Coprinus cinereus, Pleurotus flabellatus and Volvariella volvocea on composted sisal decortications residue in Tanzania’, African Journal of Biotechnology, 7(24), pp. 4551– 4562. doi: 10.5897/AJB08.792.

Nsabagasani, C., Nsengimana, S. and Hakizimana, E. (2008) Biodiversity survey in Akanyaru wetlands, unprotected important bird areas in Rwanda. Kigali, Rwanda.

Okoro, I. . and Achuba, F. . (2012) ‘Proximate and mineral analysis of some wild edible mushrooms’, African Journal of Biotechnology, 11(30), pp. 7720–7724. doi: 10.5897/AJB11.590.

Olson, D. H. et al. (2007) ‘Biodiversity management approaches for stream-riparian areas: Perspectives for Pacific Northwest headwater forests, microclimates, and amphibians’, Forest Ecology and Management, 246(1 SPEC. ISS.), pp. 81–107. doi: 10.1016/j.foreco.2007.03.053.

Opige, M. et al. (2006) ‘Indigenous knowledge and Usage of Indigenous Edible Mushrooms among the Teso People of Eastern Uganda’, Journal of Food Technology 4(4) 325-330.

Osarenkhoe, O. O., John, O. A. and Theophilus, D. A. (2014) ‘Ethnomycological Conspectus of West African Mushrooms : An Awareness Document’, Advances in microbiology, 4(January), pp. 39–54. doi: 10.4236/aim.2014.41008.

Osemwegie, O. O., Okhuoya, A. J. and Dania Akande, T. (2014) ‘Ethnomycological Conspectus of West African Mushrooms: An Awareness Document’, Advances in Microbilogy, 4(3), pp. 39–54. doi: 10.3732/ajb.1000298.

Oyetayo, O. V. (2011) ‘Medicinal uses of mushrooms in Nigeria: Towards full and sustainable exploitation’, African Journal of Traditional, Complementary and Alternative Medicines, 8(3), pp. 267–274. doi: 10.4314/ajtcam.v8i3.65289.

22

Peay, K. G. et al. (2007) ‘A strong species-area relationship for eukaryotic soil microbes: Island size matters for ectomycorrhizal fungi’, Ecology Letters, 10(6), pp. 470–480. doi: 10.1111/j.1461-0248.2007.01035.x.

Plumptre, A. J. et al. (2003) The Biodiversity of the Alberine Rift. Albertine Rift Technical Reports No.3. Wildlife Conservation Society.

REMA (2010) Rwanda State of Environment and outlook: Our Environment for Economic Development. Kigali, Rwanda.

REMA (2011) Inventories of Kivu Lake Islands Biodiversity In Support To Their Inclusion Into The Protected Areas Network In Rwanda (Karongi District)., WD info. Kigali, Rwanda. doi: 10.1002/ejoc.201200111.

REMA (2014a) Conservation plan of Lake Kivu Islands in support of their inclusion into the protected areas network in Rwanda. Kigali, Rwanda. Available at: United Nations Convention on Biological Diversity (CBD, 2011).

REMA (2014b) Fifth National Report To the Convention on Biological Diversity. Kigali, Rwanda. doi: 10.1044/leader.PPL.20012015.20.

Sandhya, D., Surendra, S. and Kumar, T. M. (2017) ‘Study of Frequency , Density , Abundance and Diversity of Wild Mushrooms of Tropical Mixed Forest of Central India’, 2(2), pp. 136–145.

Stuart, S. N., Adams, R. j. and Jenkins, M. D. (1990) Biodiversity in Sub-Saharan Africa and its islands : conservation, management, and sustainable use, Occasional papers of the IUCN Species Survival Commission ; 6. IUCN.

Tibuhwa, D. D. (2012) ‘Folk and use of mushrooms in communities around Ngorongoro and Serengeti National Park, Tanzania’, Journal of Ethnobiology and Ethnomedicine. Journal of Ethnobiology and Ethnomedicine, 8(1), p. 36. doi: 10.1186/1746- 4269-8-36.

USAID (2014) Rwanda Environmental Threats and Opportunities Assessment (ETOA). Kigali, Rwanda.

Verbeken, A. and Buyck, B. (2002) ‘Diversity and Ecology of Tropical Ectomycorrhizal Fungi in Africa’, Tropical Mycology, 1, pp. 11–24.

Wood, D. A. (2014) Structure, paleolimnology and basin history of the East Kivu graben, Lake Kivu, Rwanda from offshore seismic reflection data. Syracuse University.

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Appendix 1. List of species collected and identified in riparian zone of Kivu Lake

Specimen number Species Family Nyakarwa Mariri Mpangara Garden EM 15 Agaricus crocopeplus Agaricaceae x EM76 Agaricus sp. 1 Agaricaceae x EM 23 Agaricus sp. 2 Agaricaceae x EM67 Agaricus sp. 3 Agaricaceae x EM 38 Agaricus sp. 4 Agaricaceae x EM 110 Amanita sp. Amanitaceae x EM 11 Cantharellus sp. Cantharellaceae x Chlorophyllum EM 6 hortense Agaricaceae x EM 28 Clitocybe sp. 1 Tricholomataceae x EM 85& 57 Clitocybe sp. 2 Tricholomataceae x EM 59 &77 Clitocybe sp. 3 Tricholomataceae x EM 1 Collybia piperata Tricholomataceae x x x EM93 Collybia sp. Tricholomataceae x EM 21 Coprinus sp. 2 Agaricaceae x x x EM 12 Coprinus sp.1 Agaricaceae x x EM 33 Cotylidia aurantiaca Repetobasidiaceae x EM 51 Cyathus stercoreus Nidulariaceae x x EM 96 Entoloma sp. Entolomataceae x EM 31 Ganoderma sp. Ganodermataceae x x EM 64 Geastrum sp 1 Geastraceae x EM 68 Geastrum sp 2 Geastraceae x EM 41 Gymnopilus sp. Strophariaceae x EM70 Gymnopilus sp. Strophariaceae x EM 19 Gymnopilus zenkeri Strophariaceae x x Hygrocybe EM 14 nigrescens Hygrophoraceae x EM 46 Hygrophoropsis sp Hygrophoropsidaceae x EM101 Inocybe sp. Inocybaceae x Lentinus EM 52 brunneofloccosus Polyporaceae x EM30 Lepiota sp. 1 Agaricaceae x EM56 Lepiota sp. 2 Agaricaceae x EM63 Lepiota sp. 3 Agaricaceae x EM94 Lepiota sp. 4 Agaricaceae x EM 100 Lepiota sp. 5 Agaricaceae x x EM 40 Lepista sordida Tricholomataceae x EM 43 Lepista sp. Tricholomataceae x EM83 Lepista sp. Tricholomataceae x

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Appendix 1(continued). List of species collected and identified in riparian zone of Kivu Lake

Specimen number Species Family Nyakarwa Mariri Mpangara Garden EM 86 Leucoagaricus sp Agaricaceae x EM102 Lycoperdon sp. Agaricaceae x Macrolepiota EM 53 africana Agaricaceae x Macrolepiota EM 27 procera Agaricaceae x EM 10 Macrolepiota sp Agaricaceae x Marasmius EM 92 arborescens Marasmiaceae x EM24 Marasmius sp Marasmiaceae x x x EM 91 Mycena sp Mycenaceae x EM 4 Panaeolus sp Bolbitiaceae x x x EM 2 Parasola plicatilis Psathyrellaceae x x x x EM 109 Phlebopus sudanicus Boletinellaceae x EM 18 Pholiota sp Strophariaceae x x x EM 73 Pisolithus tinctorius Sclerodermataceae x EM 45 Pleurotus sp2 Pleurotaceae x EM 36 Psathyrella sp Psathyrellaceae x x x EM 5 Psathyrella sp Psathyrellaceae x EM49 Psathyrella sp. Psathyrellaceae x x x EM62 Psathyrella sp. Psathyrellaceae x EM 29 Ramaria sp. Gomphaceae x x x EM 99 Russula sp. Russulaceae x Schizophyllum EM 32 commune Schizophyllaceae x EM 37 Suillus granulatus Boletinellaceae x x x Termitomyces EM 44 medius Lyophyllaceae x Termitomyces EM 3 microcarpus Lyophyllaceae x x EM 13 Termitomyces &17 robustus Lyophyllaceae x EM25 Tricholoma sp. Tricholomataceae x EM54 Tricholomopsis sp. Tricholomataceae x EM 42 Volvariella volvacea Pluteaceae x

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Appendix 2. Seasonal distribution of species recorded and collected during the study.

Species Sep Oct Nov Dec Jan Feb Mar Apr May Jun Agaricus crocopeplus x Agaricus sp. 1 x Agaricus sp. 2 x Agaricus sp. 3 x Agaricus sp. 4 x Amanita sp. x Cantharellus sp. x Chlorophyllum hortense x x x Clitocybe sp. 1 x x Clitocybe sp. 2 x x Clitocybe sp. 3 x Collybia piperata x x x x x x Collybia sp. x Coprinus sp. 2 x x x x x x Coprinus sp.1 x x Cotylidia aurantiaca x x x Cyathus stercoreus x x x Entoloma sp. x Ganoderma sp. x x x Geastrum sp 1 x Geastrum sp 2 x Gymnopilus sp. x Gymnopilus sp. x Gymnopilus zenkeri x x x x x Hygrocybe nigrescens x Hygrophoropsis sp x Inocybe sp. x Lentinus brunneofloccosus x Lepiota sp. 1 x x Lepiota sp. 2 x Lepiota sp. 3 x Lepiota sp. 4 x Lepiota sp. 5 x x Lepista sordida x Lepista sp.1 x Lepista sp.2 x Leucoagaricus sp x Lycoperdon sp. x Macrolepiota africana x Macrolepiota procera x Macrolepiota sp x

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Appendix 2. (continued). Seasonal distribution of Species recorded and collected during the study.

Species Sep Oct Nov Dec Jan Feb Mar Apr May Jun Marasmius arborescens x Marasmius sp x x x x x Mycena sp x x x x Panaeolus sp x x Parasola plicatilis x x x x x x x Phlebopus sudanicus x Pholiota sp x x x x x Pisolithus tinctorius x x Pleurotus sp2 x Psathyrella sp. 1 x x x x x Psathyrella sp. 2 x x x x Psathyrella sp. 3 x x x x Psathyrella sp. 4 x Ramaria sp. x x Russula sp. x Schizophyllum commune x x x x Suillus granulatus x x x x x Termitomyces medius x Termitomyces microcarpus x x x x Termitomyces robustus x x x x x Tricholoma sp. x x Tricholomopsis sp. x Volvariella volvacea x

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Appendix 3. Provisional list of mushroom species recorded in Rwanda.

Species Family Reference

Agaricus arvensis Schaeff Agaricaceae Degreef et.al. (2016) Agaricus crocopeplus Berk. & Broome Agaricaceae Present study Agaricus sp. 1 Agaricaceae Present study Agaricus sp. 2 Agaricaceae Present study Agaricus sp. 3 Agaricaceae Present study Agaricus sp. 4 Agaricaceae Present study Agaricus sylvicola (Vitt.) Lév. Agaricaceae Degreef et.al. (2016) Amanita sp. Amanitaceae Present study borealis Marxmüller & Degreef et.al. (2016) Korhonen Armillaria cepistipes Velen. Physalacriaceae Degreef et.al. (2016) Armillaria heimii Pegler Physalacriaceae Degreef et.al. (2016) Armillaria lutea Gillet Physalacriaceae Degreef et.al. (2016) Armillaria ostoyae (Romagn.) Herink Physalacriaceae Degreef et.al. (2016) Armillaria tabescens (Scop.) Emel Physalacriaceae Degreef et.al. (2016) Auricularia auricula-judae (Bull.) Quél. Auriculariaceae Degreef et.al. (2016)

Auricularia cornea Ehrenb. Auriculariaceae Degreef et.al. (2016) Auricularia delicata (Mont. ex Fr.) Henn. Auriculariaceae Degreef et.al. (2016)

Cantharellus sp. Cantharellaceae Present study Chlorophyllum hortense (Murrill) Vellinga Agaricaceae Present study

Clitocybe sp. 1 Tricholomataceae Present study Clitocybe sp. 2 Tricholomataceae Present study Clitocybe sp. 3 Tricholomataceae Present study Collybia aurea (Beeli) Pegler Tricholomataceae Degreef et.al. (2016) Collybia piperata (Beeli) Singer Tricholomataceae Present study Collybia sp. Tricholomataceae Present study Coprinus sp. 2 Agaricaceae Present study Coprinus sp.1 Agaricaceae Present study Cotylidia aurantiaca (Pat.) A.L. Welden Repetobasidiaceae Present study, Degreef et.al. (2016) Cyathus stercoreus (Schwein.) De Toni Nidulariaceae Present study Cystodermella elegans (Beeli) Harmaja Agaricaceae Degreef et.al. (2016) Dacryopinax spathularia (Schwein.) G.W. Dacrymycetaceae Degreef et.al. (2016) Martin Entoloma sp. Entolomataceae Present study Ganoderma sp. Ganodermataceae Present study Geastrum sp 1 Geastraceae Present study Geastrum sp 2 Geastraceae Present study Gymnopilus sp.1 Strophariaceae Present study

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Appendix 3 (continued). Provisional list of mushroom species recorded in Rwanda

Species Family Reference

Gymnopilus sp.2 Strophariaceae Present study Gymnopilus zenkeri (Henn.) Singer Strophariaceae Present study Hygrocybe nigrescens (Quél.) Kühner Hygrophoraceae Present study Hygrophoropsis sp. Hygrophoropsidaceae Present study Hypholoma subviride (Berk. & M.A. Strophariaceae Degreef et.al. (2016) Curtis) Dennis Inocybe sp. Inocybaceae Present study Lentinus brunneofloccosus Pegler Polyporaceae Present study Lentinus cladopus Lév. Polyporaceae Degreef et.al. (2016) Lentinus retinervis Pegler Polyporaceae Degreef et.al. (2016) Lentinus sajor-caju (Fr.) Fr. Polyporaceae Degreef et.al. (2016) Lepiota sp. 1 Agaricaceae Present study Lepiota sp. 2 Agaricaceae Present study Lepiota sp. 3 Agaricaceae Present study Lepiota sp. 4 Agaricaceae Present study Lepiota sp. 5 Agaricaceae Present study Lepista sordida (Schumach.) Singer Tricholomataceae Present study, Degreef et.al. (2016) Lepista sp.1 Tricholomataceae Present study Lepista sp.2 Tricholomataceae Present study Leucoagaricus sp. Agaricaceae Present study Lycoperdon sp. Agaricaceae Present study Macrolepiota africana (R.Heim) Heinem. Agaricaceae Present study, Degreef et.al. (2016) Macrolepiota dolichaula (Berk. & Agaricaceae Degreef et.al. (2016) Broome) Pegler & R.W. Rayner Macrolepiota procera (Scop.) Singer Agaricaceae Present study Macrolepiota sp. Agaricaceae Present study Marasmiellus inoderma (Berk.) Singer Marasmiaceae Degreef et.al. (2016) Marasmius arborescens (Henn.) Beeli Marasmiaceae Present study, Degreef et.al. (2016) Marasmius bekolacongoli Beeli Marasmiaceae Degreef et.al. (2016) Marasmius sp. Marasmiaceae Present study Mycena sp. Mycenaceae Present study Panaeolus sp. Bolbitiaceae Present study Parasola plicatilis (Curtis) Redhead et al Psathyrellaceae Present study Paxillus brunneotomentosus Heinem. & Paxillaceae Degreef et.al. (2016) Rammeloo Phlebopus sudanicus (Har. & Pat.) Boletinellaceae Present study Heinem. Pholiota sp. Strophariaceae Present study Pisolithus tinctorius Coker & Couch Sclerodermataceae Present study Pleurotus cystidiosus O.K. Mill. Pleurotaceae Degreef et.al. (2016)

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Appendix 3 (continued). Provisional list of mushroom species recorded in Rwanda

Species Family Reference

Pleurotus djamor (Rumph. ex Fr.) Boedijn Pleurotaceae Degreef et.al. (2016) Pleurotus flabellatus Sacc. Pleurotaceae Degreef et.al. (2016) Pleurotus sp.1 Pleurotaceae Present study Polyporus tenuiculus (P. Beauv.) Fr Polyporaceae Degreef et.al. (2016) Psathyrella atroumbonata Pegler Psathyrellaceae Degreef et.al. (2016) Psathyrella sp. 1 Psathyrellaceae Present study Psathyrella sp. 2 Psathyrellaceae Present study Psathyrella sp. 3 Psathyrellaceae Present study Psathyrella sp. 4 Psathyrellaceae Present study Psathyrella tuberculata (Path.) A.H. Sm. Psathyrellaceae Degreef et.al. (2016) Ramaria sp. Gomphaceae Present study Russula sp. Russulaceae Present study Schizophyllum commune Fr. Schizophyllaceae Present study Suillus granulatus (L.) Roussel Boletinellaceae Present study, Degreef et.al. (2016) Termitomyces medius R. Heim & Grassé Lyophyllaceae Present study Termitomyces microcarpus (Berk. & Lyophyllaceae Present study, Degreef et.al. (2016) Broome) R. Heim Termitomyces robustus (Beeli) R. Heim Lyophyllaceae Present study, Degreef et.al. (2016)

Termitomyces schimperi (Pat.) R. Heim Lyophyllaceae Degreef et.al. (2016) Termitomyces striatus (Beeli) R. Heim Lyophyllaceae Degreef et.al. (2016) Tricholoma sp. Tricholomataceae Present study Tricholomopsis sp. Tricholomataceae Present study Volvariella volvacea (Bul.) Singer Pluteaceae Present study

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Appendix 4. Photo of some species collected and identified.

1. Agaricus crocopeplus, 2. Agaricus sp., 3. Agaricus sp., 4. Amanita sp., 5. Cantharellus sp., 6. Chlorophyllum hortense, 7. Clitocybe sp., 8. Clitocybe sp., 9. Collybia piperata, 10. Coprinus sp., 11. Coprinus sp., 12. Cotylidia aurantiaca

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Appendix 4 (continued). Photos of some species collected and identified.

13. Cyathus stercoreus, 14. Entoloma sp. , 15. Ganoderma sp., 16. Geastrum sp. 17. Geastrum sp., 18. Gymnopilus sp., 19. Gymnopilus zenkeri 20. Hygrocybe nigrescens, 21. Hygrophoropsis sp., 22. Lentinus brunneofloccosus 23. Lepiota sp., 24. Lepista sordida

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Appendix 4 (continued). Photos of some species collected and identified.

25. Lepista sp. 26. Leucoagaricus sp. 27. Macrolepiota africana, 28. Macrolepiota procera 29. Marasmius arborescens 30. Mycena sp. 31. Panaeolus sp. 32. Parasola plicatilis 33. Phlebopus sudanicus 34. Pholiota sp. 35. Pisolithus tinctorius 36. Pleurotus sp.

33

Appendix 4 (continued). Photos of some species collected and identified.

37. Psathyrella sp. 38. Psathyrella sp 2. 39. Ramaria sp. 40. Russula sp. 41. Schizophyllum commune 42. Suillus granulatus 43. Termitomyces medius 44. Termitomyces microcarpus 45. Termitomyces robustus 46. Volavariella volvacea

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Appendix 5. Distribution of mushroom species in different habitat types

Species Habitat types Forest Grassland Woodland Garden Agaricus crocopeplus x Agaricus sp. 1 x Agaricus sp. 2 x Agaricus sp. 3 x Agaricus sp. 4 x Amanita sp. x Cantharellus sp. x Chlorophyllum hortense x Clitocybe sp. 1 x Clitocybe sp. 2 x Clitocybe sp. 3 x Collybia piperata x x Collybia sp. x Coprinus sp. 2 x x Coprinus sp.1 x x Cotylidia aurantiaca x Cyathus stercoreus x x Entoloma sp. x Ganoderma sp. x Geastrum sp. 1 x Geastrum sp. 2 x Gymnopilus sp. 1 x Gymnopilus sp.2 x Gymnopilus zenkeri x x x Hygrocybe nigrescens x Hygrophoropsis sp. x Inocybe sp. x Lentinus brunneofloccosus x Lepiota sp. 1 x Lepiota sp. 2 x Lepiota sp. 3 x Lepiota sp. 4 x Lepiota sp. 5 x x Lepista sordida x Lepista sp. 1 x Lepista sp. 2 x Leucoagaricus sp x Lycoperdon sp. x Macrolepiota africana x Macrolepiota procera x Macrolepiota sp. x x

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Appendix 5 (Continued). Distribution of mushroom species in different habitat types

Species Habitat types Forest Grassland Woodland Garden Marasmius arborescens x Marasmius sp. x Mycena sp. x Panaeolus sp. x x Parasola plicatilis x x x x Phlebopus sudanicus x x Pholiota sp. x x x Pisolithus tinctorius x Pleurotus sp2 x Psathyrella sp. 1 x x Psathyrella sp. 2 x Psathyrella sp. 3 x x x Psathyrella sp. 4 x Ramaria sp. x x Russula sp. x Schizophyllum commune x Suillus granulatus x x x Termitomyces medius x Termitomyces microcarpus x x Termitomyces robustus x Tricholoma sp. x Tricholomopsis sp. x Volvariella volvacea x

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